Treating cattle with antibiotics affects greenhouse gas emissions, and microbiota in dung and dung beetles

Abstract

Antibiotics are routinely used to improve livestock health and growth. However, this practice may have unintended environmental impacts mediated by interactions among the wide range of micro-and macroorganisms found in agroecosystems. For example, antibiotics may alter microbial emissions of greenhouse gases by affecting livestock gut microbiota. Furthermore, antibiotics may affect the microbiota of non-target animals that rely on dung, such as dung beetles, and the ecosystem services they provide. To examine these interactions, we treated cattle with a commonly used broad-spectrum antibiotic and assessed downstream effects on microbiota in dung and dung beetles, greenhouse gas fluxes from dung, and beetle size, survival and reproduction. We found that antibiotic treatment restructured microbiota in dung beetles, which harboured a microbial community distinct from those in the dung they were consuming. The antibiotic effect on beetle microbiota was not associated with smaller size or lower numbers. Unexpectedly, antibiotic treatment raised methane fluxes from dung, possibly by altering the interactions between methanogenic archaea and bacteria in rumen and dung environments. Our findings that antibiotics restructure dung beetle microbiota and modify greenhouse gas emissions from dung indicate that antibiotic treatment may have unintended, cascading ecological effects that extend beyond the target animal.

The role of livestock intensification and landscape structure in maintaining tropical biodiversity

“…Although the impact of livestock management on dung beetle assemblages seems to be weaker than that of landscape structure, the use of macrocyclic lactones is strongly and negatively related to all response variables. This supports previous work showing that macrocyclic lactones have negative effects on the ecology and biology of different soil invertebrate taxa, including mites, springtails, earthworms, flies, wasps (Hammer et al., ; Jochmann & Blanckenhorn, ) and dung beetles (Basto‐Estrella et al., ). These negative effects are related to the accumulation of macrocyclic lactones in cattle dung, changing their nutritional, chemical and microbiological properties (Hammer et al., ; Jochmann & Blanckenhorn, ).…”

“…This supports previous work showing that macrocyclic lactones have negative effects on the ecology and biology of different soil invertebrate taxa, including mites, springtails, earthworms, flies, wasps (Hammer et al., ; Jochmann & Blanckenhorn, ) and dung beetles (Basto‐Estrella et al., ). These negative effects are related to the accumulation of macrocyclic lactones in cattle dung, changing their nutritional, chemical and microbiological properties (Hammer et al., ; Jochmann & Blanckenhorn, ). Such contaminated dung can produce landscape‐scale toxicological effects, even at low concentrations (Jochmann & Blanckenhorn, ).…”

“…Finally, the use of agrochemicals, such as fertilizers and veterinary medicines, which may be higher in high‐yielding agricultural landscapes, can also exert significant influences on biodiversity (Hammer et al., ). These effects can be seen both on‐ and off‐farm (Jochmann & Blanckenhorn, ; Thornton et al., ) and we predicted that the use of macrocyclic lactones would have strong negative effects on dung beetle communities.…”

Review of Antimicrobial Resistance in the Environment and Its Relevance to Environmental Regulators

“…On-farm transmission of AMR has been characterized in the literature for a wide range of animals: pigs (Crombé et al, 2013; Novais et al, 2013), cows (Wichmann et al, 2014), and insects (Zurek and Ghosh, 2014; Usui et al, 2015; Hammer et al, 2016). A recent review of the academic literature that address the issue of antibiotic use in agriculture suggests that only seven studies (five percent) argued that there was no link between antibiotic consumption in animals and resistance in humans, while 100 (72%) found evidence of a link (O’Neill and The Review on Antimicrobial Resistance, 2015).…”

Contribution of organic farming to public goods in Denmark

“…Recent studies have shown that antibiotics may significantly affect the microbiota in dung and dung beetles negatively (Hammer et al 2017). In Denmark, more than half (57.1%) of the dung beetles are listed on the Danish Redlist (Department of Bioscience 2017), and one of the reasons for this may be the extensive use of antibiotics for livestock.…”